The Effects of Mechanical Loading on Mesenchymal Stem Cell Differentiation and Matrix Production

Vitamins and Hormones

Volumn 87, Issue , 2011, Pages 417-480

  Delaine Smith, Robin M ^a   Reilly, Gwendolen C ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

Adipogenesis; Bioreactor; Chondrogenesis; Extracellular matrix; Fluid flow; Mechanotransduction; Mesenchymal stem cells; Osteogenesis; Tenogenesis

Indexed keywords

EID: 84857134964     PISSN: 00836729     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-386015-6.00039-1     Document Type: Chapter

References (190)

1. Altman G.H., Horan R.L., Martin I., Farhadi J., Stark P.R.H., Volloch V., Richmond J.C., Vunjak-Novakovic G., Kaplan D.L. Cell differentiation by mechanical stress. FASEB J. 2002, 16:270-272.
2. Anderson E.J., Tate M.L.K. Open access to novel dual flow chamber technology for in vitro cell mechanotransduction, toxicity and pharamacokinetic studies. Biomed. Eng. Online 2007, 6:46.
3. Angele P., Yoo J.U., Smith C., Mansour J., Jepsen K.J., Nerlich M., Johnstone B. Cyclic hydrostatic pressure enhances the chondrogenic phenotype of human mesenchymal progenitor cells differentiated in vitro. J. Orthop. Res. 2003, 21:451-457.
4. Angele P., Schumann D., Angele M., Kinner B., Englert C., Hente R., Fuchtmeier B., Nerlich M., Neumann C., Kujat R. Cyclic, mechanical compression enhances chondrogenesis of mesenchymal progenitor cells in tissue engineering scaffolds. Biorheology 2004, 41:335-346.
5. Angle S.R., Sena K., Sumner D.R., Virdi A.S. Osteogenic differentiation of rat bone marrow stromal cells by various intensities of low-intensity pulsed ultrasound. Ultrasonics 2011, 51:281-288.
6. Antonitsis P., Ioannidou-Papagiannaki E., Kaidoglou A., Papakonstantinou C. In vitro cardiomyogenic differentiation of adult human bone marrow mesenchymal stem cells. The role of 5-azacytidine. Interact. Cardiovasc. Thorac. Surg. 2007, 6:593-597.
7. Archer R., Williams D.J. Why tissue engineering needs process engineering. Nat. Biotechnol. 2005, 23:1353-1355.
8. Arnsdorf E.J., Tummala P., Kwon R.Y., Jacobs C.R. Mechanically induced osteogenic differentiation--The role of RhoA, ROCKII and cytoskeletal dynamics. J. Cell Sci. 2009, 122:546-553.
9. Augello A., De Bari C. The regulation of differentiation in mesenchymal stem cells. Hum. Gene Ther. 2010, 21:1226-1238.
10. Augst A., Marolt D., Freed L.E., Vepari C., Meinel L., Farley M., Fajardo R., Patel N., Gray M., Kaplan D.L., Vunjak-Novakovic G. Effects of chondrogenic and osteogenic regulatory factors on composite constructs grown using human mesenchymal stem cells, silk scaffolds and bioreactors. J. R. Soc. Interface 2008, 5:929-939.
11. Bakker A.D., Soejima K., Klein-Nulend J., Burger E.H. The production of nitric oxide and prostaglandin E-2 by primary bone cells is shear stress dependent. J. Biomech. 2001, 34:671-677.
12. Bancroft G.N., Sikavitsast V.I., van den Dolder J., Sheffield T.L., Ambrose C.G., Jansen J.A., Mikos A.G. Fluid flow increases mineralized matrix deposition in 3D perfusion culture of marrow stromal osteloblasts in a dose-dependent manner. Proc. Natl. Acad. Sci. USA 2002, 99:12600-12605.
13. Bassey E.J., Ramsdale S.J. Increase in femoral bone density in young women following high impact exercise. Osteoporos. Int. 1994, 4:72-75.
14. Batra N.N., Li Y.J., Yellowley C.E., You L.D., Malone A.M., Kim C.H., Jacobs C.R. Effects of short-term recovery periods on fluid-induced signaling in osteoblastic cells. J. Biomech. 2005, 38(9):1909-1917.
15. Ben-David U., Benvenisty N. The tumorigenicity of human embryonic and induced pluripotent stem cells. Nat. Rev. Cancer 2011, 11:268-277.
16. Beresford J.N., Bennett J.H., Devlin C., Leboy P.S., Owen M.E. Evidence for an inverse relationship between the differentiation of adipocytic and osteogenic cells in rat marrow stromal cell-cultures. J. Cell Sci. 1992, 102:341-351.
17. Bonewald L.F., Johnson M.L. Osteocytes, mechanosensing and Wnt signaling. Bone 2008, 42:606-615.
18. Brown T.D. Techniques for mechanical stimulation of cells in vitro: A review. J. Biomech. 2000, 33:3-14.
19. Byrne E.M., Farrell E., McMahon L.A., Haugh M.G., O'Brien F.J., Campbell V.A., Prendergast P.J., O'Connell B.C. Gene expression by marrow stromal cells in a porous collagen-glycosaminoglycan scaffold is affected by pore size and mechanical stimulation. J. Mater. Sci. Mater. Med. 2008, 19:3455-3463.
20. Case N., Sen B., Thomas J.A., Styner M., Xie Z., Jacobs C.R., Rubin J. Steady and oscillatory fluid flows produce a similar osteogenic phenotype. Calcif. Tissue Int. 2011, 88:189-197.
21. Chanda D., Kumar S., Ponnazhagan S. Therapeutic potential of adult bone marrow derived mesenchymal stem cells in diseases of the skeleton. J. Cell. Biochem. 2010, 111:249-257.
22. Chang Y.L., Stanford C.M., Keller J.C. Calcium and phosphate supplementation promotes bone cell mineralization: Implications for hydroxyapatite (HA)-enhanced bone formation. J. Biomed. Mater. Res. 2000, 52:270-278.
23. Chen Y.J., Huang C.H., Lee I.C., Lee Y.T., Chen M.H., Young T.H. Effects of cyclic mechanical stretching on the mRNA expression of tendon/ligament-related and osteoblast-specific genes in human mesenchymal stem cells. Connect. Tissue Res. 2008, 49:7-14.
24. Cioffi M., Boschetti F., Raimondi M.T., Dubini G. Modeling evaluation of the fluid-dynamic microenvironment in tissue-engineered constructs: A micro-CT based model. Biotechnol. Bioeng. 2006, 93:500-510.
25. Colazzo F., Sarathchandra P., Smolenski R.T., Chester A.H., Tseng Y.T., Czernuszka J.T., Yacoub M.H., Taylor P.M. Extracellular matrix production by adipose-derived stem cells: Implications for heart valve tissue engineering. Biomaterials 2010, 32:119-127.
26. Colley H.E., Mishra G., Scutt A.M., McArthur S.L. Plasma polymer coatings to support mesenchymal stem cell adhesion, growth and differentiation on variable stiffness silicone elastomers. Plasma Process. Polym. 2009, 6:831-839.
27. Connelly J.T., Vanderploeg E.J., Mouw J.K., Wilson C.G., Levenston M.E. Tensile loading modulates bone marrow stromal cell differentiation and the development of engineered fibrocartilage constructs. Tissue Eng. Part A 2010, 16:1913-1923.
28. Dalby M.J., Gadegaard N., Tare R., Andar A., Riehle M.O., Herzyk P., Wilkinson C.D.W., Oreffo R.O.C. The control of human mesenchymal cell differentiation using nanoscale symmetry and disorder. Nat. Mater. 2007, 6(12):997-1003.
29. Datta N., Pham Q.P., Sharma U., Sikavitsas V.I., Jansen J.A., Mikos A.G. In vitro generated extracellular matrix and fluid shear stress synergistically enhance 3D osteoblastic differentiation. Proc. Natl. Acad. Sci. USA 2006, 103:2488-2493.
30. De Bari C., Dell'Accio F., Luyten F.P. Human periosteum-derived cells maintain phenotypic stability and chondrogenic potential throughout expansion regardless of donor age. Arthritis Rheum. 2001, 44:85-95.
31. Delaine-Smith R.M., MacNeil S., Reilly G.C. Osteogenic media and fluid shear forces can induce osteogenic differentiation in dermal fibroblasts. Trans. Annu. Meet. Orthop. Res. Soc. 2011, 57. Long Beach, California.
32. Deligianni D.D., Katsala N.D., Koutsoukos P.G., Missirlis Y.F. Effect of surface roughness of hydroxyapatite on human bone marrow cell adhesion, proliferation, differentiation and detachment strength. Biomaterials 2001, 22:87-96.
33. Della Rocca G.J. The science of ultrasound therapy for fracture healing. Indian J. Orthop. 2009, 43:121-126.
34. Diefenderfer D.L., Osyczka A.M., Reilly G.C., Leboy P.S. BMP responsiveness in human mesenchymal stem cells. Connect. Tissue Res. 2003, 44:305-311.
35. Dominici M., Le Blanc K., Mueller I., Slaper-Cortenbach I., Marini F.C., Krause D.S., Deans R.J., Keating A., Prockop D.J., Horwitz E.M. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006, 8:315-317.
36. Donahue T.L.H., Haut T.R., Yellowley C.E., Donahue H.J., Jacobs C.R. Mechanosensitivity of bone cells to oscillating fluid flow induced shear stress may be modulated by chemotransport. J. Biomech. 2003, 36:1363-1371.
37. Dumas V., Ducharne B., Perrier A., Fournier C., Guignandon A., Thomas M., Peyroche S., Guyomar D., Vico L., Rattner A. Extracellular matrix produced by osteoblasts cultured under low-magnitude, high-frequency stimulation is favorable to osteogenic differentiation of mesenchymal stem cells. Calcif. Tissue Int. 2010, 87:351-364.
38. Duty A.O., Oest M.E., Guldberg R.E. Cyclic mechanical compression increases mineralization of cell-seeded polymer scaffolds in vivo. J. Biomech. Eng. Trans. ASME 2007, 129:531-539.
39. Edwards J.H., Reilly G.C. Low magnitude, high frequency vibration modulates mesenchymal progenitor differentiation. Trans. Annu. Meet. Orthop. Res. Soc. 2011, 57. Long Beach, California.
40. El Haj A.J., Cartmell S.H. Bioreactors for bone tissue engineering. Proc. Inst. Mech. Eng. H 2010, 224:1523-1532.
41. Engler A.J., Sen S., Sweeney H.L., Diskher D.E. Matrix elasticity directs stem cell lineage specification. Cell 2006, 126:677-689.
42. Erices A., Conget P., Minguell J.J. Mesenchymal progenitor cells in human umbilical cord blood. Br. J. Haematol. 2000, 109:235-242.
43. Fan X.F., Zou R., Zhao Z.H., Yang P., Li Y., Song J.L. Tensile strain induces integrin beta 1 and ILK expression higher and faster in 3D cultured rat skeletal myoblasts than in 2D cultures. Tissue Cell 2009, 41:266-270.
44. Farng E., Urdaneta A.R., Barba D., Esmende S., McAllister D.R. The effects of GDF-5 and uniaxial strain on mesenchymal stem cells in 3-D culture. Clin. Orthop. Relat. Res. 2008, 466:1930-1937.
45. Finger A.R., Sargent C.Y., Dulaney K.O., Bernacki S.H., Loboa E.G. Differential effects on messenger ribonucleic acid expression by bone marrow-derived human mesenchymal stem cells seeded in agarose constructs due to ramped and steady applications of cyclic hydrostatic pressure. Tissue Eng. 2007, 13:1151-1158.
46. Frangos J.A., McIntire L.V., Eskin S.G. Shear stress induced stimulation of mammalian cell metabolisam. Biotechnol. Bioeng. 1988, 32:1053-1060.
47. Friedenstein A.J., Piatetzky-Shapiro I.I., Petrakova K.V. Osteogenesis in transplants of bone marrow cells. J. Embryol. Exp. Morphol. 1966, 16:381-390.
48. Gelse K., von der Mark K., Aigner T., Park J., Schneider H. Articular cartilage repair by gene therapy using growth factor-producing mesenchymal cells. Arthritis Rheum. 2003, 48:430-441.
49. Gilbert J.A., Weinhold P.S., Banes A.J., Link G.W., Jones G.L. Strain profiles for circular cell culture plates containing flexible surfaces employed to mechanically deform cells in vitro. J. Biomech. 1994, 27:1169-1177.
50. 2+ flux in fibroblasts. Am. J. Physiol. Cell Physiol. 1995, 269:C1093-C1104.
51. Glossop J.R., Cartmell S.H. Effect of fluid flow-induced shear stress on human mesenchymal stem cells: Differential gene expression of IL1B and MAP3K8 in MAPK signaling. Gene Expr. Patterns 2009, 9:381-388.
52. Gomes M.E., Sikavitsas V.I., Behravesh E., Reis R.L., Mikos A.G. Effect of flow perfusion on the osteogenic differentiation of bone marrow stromal cells cultured on starch-based three-dimensional scaffolds. J. Biomed. Mater. Res. A 2003, 67A:87-95.
53. Goodwin H.S., Bicknese A.R., Chien S.N., Bogucki B.D., Oliver D.A., Quinn C.O., Wall D.A. Multilineage differentiation activity by cells isolated from umbilical cord blood: Expression of bone, fat, and neural markers. Biol. Blood Marrow Transplant. 2001, 7:581-588.
54. Grayson W.L., Bhumiratana S., Cannizzaro C., Chao P.H.G., Lennon D.P., Caplan A.I., Vunjak-Novakovic G. Effects of initial seeding density and fluid perfusion rate on formation of tissue-engineered bone. Tissue Eng. Part A 2008, 14:1809-1820.
55. Grellier M., Bareille R., Bourget C., Amedee J. Responsiveness of human bone marrow stromal cells to shear stress. J. Tissue Eng. Regen. Med. 2009, 3:302-309.
56. Guilak F., Cohen D.M., Estes B.T., Gimble J.M., Liedtke W., Chen C.S. Control of stem cell fate by physical interactions with the extracellular matrix. Cell Stem Cell 2009, 5:17-26.
57. Gurkan U.A., Akkus O. The mechanical environment of bone marrow: A review. Ann. Biomed. Eng. 2008, 36:1978-1991.
58. Hanson A.D., Marvel S.W., Bernacki S.H., Banes A.J., van Aalst J., Loboa E.G. Osteogenic effects of rest inserted and continuous cyclic tensile strain on hASC lines with disparate osteodifferentiation capabilities. Ann. Biomed. Eng. 2009, 37:955-965.
59. Haudenschild A.K., Hsieh A.H., Kapila S., Lotz J.C. Pressure and distortion regulate human mesenchymal stem cell gene expression. Ann. Biomed. Eng. 2009, 37:492-502.
60. Henderson J.H., De la Fuente L., Romero D., Colnot C.I., Huang S., Carter D.R., Helms J.A. Rapid growth of cartilage rudiments may generate perichondrial structures by mechanical induction. Biomech. Model. Mechanobiol. 2007, 6:127-137.
61. Holtorf H.L., Jansen J.A., Mikos A.G. Flow perfusion culture induces the osteoblastic differentiation of marrow stromal cell-scaffold constructs in the absence of dexamethasone. J. Biomed. Mater. Res. A 2005, 72A:326-334.
62. Huang C.H., Chen M.H., Young T.H., Jeng J.H., Chen Y.J. Interactive effects of mechanical stretching and extracellular matrix proteins on initiating osteogenic differentiation of human mesenchymal stem cells. J. Cell. Biochem. 2009, 108:1263-1273.
63. Huang A.H., Farrell M.J., Kim M., Mauck R.L. Long term dynamic loading improves the mechanical properties of chondrogenic mesenchymal stem cell laden hydrogels. Eur. Cell. Mater. 2010, 19:72-85.
64. Huang Y., Jia X.L., Bai K., Gong X.H., Fan Y.B. Effect of fluid shear stress on cardiomyogenic differentiation of rat bone marrow mesenchymal stem cells. Arch. Med. Res. 2010, 41:497-505.
65. Hubbe M.A. Adhesion and detachment of biological cells in vitro. Prog. Surf. Sci. 1981, 11:65-138.
66. Hughes S., El Haj A.J., Dobson J. Magnetic micro- and nanoparticle mediated activation of mechanosensitive ion channels. Med. Eng. Phys. 2005, 27:754-762.
67. Ikeda K., Takayama T., Suzuki N., Shimada K., Otsuka K., Ito K. Effects of low-intensity pulsed ultrasound on the differentiation of C2C12 cells. Life Sci. 2006, 79:1936-1943.
68. Iqbal J., Zaidi M. Molecular regulation of mechanotransduction. Biochem. Biophys. Res. Commun. 2005, 328:751-755.
69. Jaasma M.J., O'Brien F.J. Mechanical stimulation of osteoblasts using steady and dynamic fluid flow. Tissue Eng. Part A 2008, 14(7):1213-1223.
70. Jacobs C.R., Yellowley C.E., Davis B.R., Zhou Z., Cimbala J.M., Donahue H.J. Differential effect of steady versus oscillating flow on bone cells. J. Biomech. 1998, 31:969-976.
71. Jagodzinski M., Drescher M., Zeichen J., Hankemeier S., Krettek C., Bosch U., van Griensven M. Effects of cyclic longitudinal mechanical strain and dexamethasone on osteogenic differentiation of human bone marrow stromal cells. Eur. Cell. Mater. 2004, 7:35-41.
72. Janmey P.A., McCulloch C.A. Cell mechanics: Integrating cell responses to mechanical stimuli. Annu. Rev. Biomed. Eng. 2007, 9:1-34.
73. Johnstone B., Hering T.M., Caplan A.I., Goldberg V.M., Yoo J.U. In vitro chondrogenesis of bone marrow-derived mesenchymal progenitor cells. Exp. Cell Res. 1998, 238:265-272.
74. Jonas O., Duschl C. Force propagation and force generation in cells. Cytoskeleton 2010, 67:555-563.
75. Jungreuthmayer C., Donahue S.W., Jaasma M.J., Al-Munajjed A.A., Zanghellini J., Kelly D.J., O'Brien F.J. A comparative study of shear stresses in collagen-glycosaminoglycan and calcium phosphate scaffolds in bone tissue-engineering bioreactors. Tissue Eng. Part A 2009, 15:1141-1149.
76. Kanczler J.M., Sura H.S., Magnay J., Green D., Oreffo R.O.C., Dobson J.P., El Haj A.J. Controlled differentiation of human bone marrow stromal cells using magnetic nanoparticle technology. Tissue Eng. Part A 2009, 16:3241-3250.
77. Kasper G., Dankert N., Tuischer J., Hoeft M., Gaber T., Glaeser J.D., Zander D., Tschirschmann M., Thompson M., Matziolis G., Duda G.N. Mesenchymal stem cells regulate angiogenesis according to their mechanical environment. Stem Cells 2007, 25:903-910.
78. Kasten A., Muller P., Bulnheim U., Groll J., Bruellhoff K., Beck U., Steinhoff G., Moller M., Rychly J. Mechanical integrin stress and magnetic forces induce biological responses in mesenchymal stem cells which depend on environmental factors. J. Cell. Biochem. 2010, 111:1586-1597.
79. Kielty C.M., Hopkinson I., Grant M.E. Collagen: The collagen family: Structure, assembly, and organization in the extracellular matrix. Connective Tissue and Its Heritable Disorders: Molecular, Genetic, and Medical Aspects 1993, 103-147. Wiley-Liss, Inc., Chichester. P.M. Royce, B. Steinmann (Eds.).
80. Kim S.H., Choi Y.R., Park M.S., Shin J.W., Park K.D., Kim S.J., Lee J.W. Erk 1/2 activation in enhanced osteogenesis of human mesenchymal stem cells in poly(lactic-glycolic acid) by cyclic hydrostatic pressure. J. Biomed. Mater. Res. A 2007, 80A:826-836.
81. Kisiday J.D., Frisbie D.D., McIlwraith C.W., Grodzinsky A.J. Dynamic compression stimulates proteoglycan synthesis by mesenchymal stem cells in the absence of chondrogenic cytokines. Tissue Eng. Part A 2009, 15:2817-2824.
82. Klein-Nulend J., Bacabac R.G., Mullender M.G. Mechanobiology of bone tissue. Pathol. Biol. 2005, 53:576-580.
83. Kobayashi Y., Sakai D., Iwashina T., Iwabuchi S., Mochida J. Low ntensity pulsed ultrasound stimulates cell proliferation, proteoglycan synthesis and expression of growth factor related genes in human nucleus pulposus cell line. Eur. Cells Mater. 2009, 17:15-22.
84. Koc O.N., Day J., Nieder M., Gerson S.L., Lazarus H.M., Krivit W. Allogeneic mesenchymal stem cell infusion for treatment of metachromatic leukodystrophy (MLD) and Hurler syndrome (MPS-IH). Bone Marrow Transplant. 2002, 30:215-222.
85. Korstjens C.M., van der Rijt R.H.H., Albers G.H.R., Semeins C.M., Klein-Nulend J. Low-intensity pulsed ultrasound affects human articular chondrocytes in vitro. Med. Biol. Eng. Comput. 2008, 46:1263-1270.
86. Kreke M.R., Goldstein A.S. Hydrodynamic shear stimulates osteocalcin expression but not proliferation of bone marrow stromal cells. Tissue Eng. 2004, 10:780-788.
87. Kreke M.R., Huckle W.R., Goldstein A.S. Fluid flow stimulates expression of osteopontin and bone sialoprotein by bone marrow stromal cells in a temporally dependent manner. Bone 2005, 36:1047-1055.
88. Ku C.H., Johnson P.H., Batten P., Sarathchandra P., Chambers R.C., Taylor P.M., Yacoub M.H., Chester A.H. Collagen synthesis by mesenchymal stem cells and aortic valve interstitial cells in response to mechanical stretch. Cardiovasc. Res. 2006, 71:548-556.
89. Kuo C.K., Tuan R.S. Mechanoactive tenogenic differentiation of human mesenchymal stem cells. Tissue Eng. Part A 2008, 14:1615-1627.
90. Lacroix D., Prendergast P.J., Li G., Marsh D. Biomechanical model to simulate tissue differentiation and bone regeneration: Application to fracture healing. Med. Biol. Eng. Comput. 2002, 40:14-21.
91. Lai C.H., Chen S.C., Chiu L.H., Yang C.B., Tsai Y.H., Zuo C.S., Chang W.H.S., Lai W.F. Effects of low intensity pulsed ultrasound, dexamethasone TGF-beta1 and/or BMP-2 on the transcriptional expression of genes in human mesenchymal stem cells: Chondrogenic vs. osteogenic differentiation. Ultrasound Med. Biol. 2010, 36:1022-1033.
92. Lee H.J., Choi B.H., Min B.H., Son Y.S., Park S.R. Low-intensity ultrasound stimulation enhances chondrogenic differentiation in alginate culture of mesenchymal stem cells. Artif. Organs 2006, 30:707-715.
93. Li Y.J., Batra N.N., You L.D., Meier S.C., Coe I.A., Yellowley C.E., Jacobs C.R. Oscillatory fluid flow affects human marrow stromal cell proliferation and differentiation. J. Orthop. Res. 2004, 22:1283-1289.
94. Li X.H., Yu X.Y., Lin Q.X., Deng C.Y., Shan Z.X., Yang M., Lin S.G. Bone marrow mesenchymal stem cells differentiate into functional cardiac phenotypes by cardiac microenvironment. J. Mol. Cell. Cardiol. 2007, 42:295-303.
95. Li D.Q., Tang T.T., Lu J.X., Dai K.R. Effects of flow shear stress and mass transport on the construction of a large-scale tissue-engineered bone in a perfusion bioreactor. Tissue Eng. Part A 2009, 15:2773-2783.
96. Li Z., Yao S.J., Alini M., Stoddart M.J. Chondrogenesis of human bone marrow mesenchymal stem cells in fibrin-polyurethane composites is modulated by frequency and amplitude of dynamic compression and shear stress. Tissue Eng. Part A 2009, 16:575-584.
97. Liedert A., Claes L., Ignatius A. Signal transduction pathways involved in mechanotransduction in osteoblastic and mesenchymal stem cells. Mechanosensitivity in Cells and Tissues 2008, 253-265. Springer, Dordrecht. A. Kamkin, I. Kiseleva (Eds.).
98. Lin T.M., Tsai J.L., Lin S.D., Lai C.S., Chang C.C. Accelerated growth and prolonged lifespan of adipose tissue-derived human mesenchymal stem cells in a medium using reduced calcium and antioxidants. Stem Cells Dev. 2005, 14:92-102.
99. Liu J., Zhao Z.H., Li J., Zou L., Shuler C., Zou Y.W., Huang X.J., Li M.L., Wang J. hydrostatic pressures promote initial osteodifferentiation With ERK1/2 Not p38 MAPK signaling involved. J. Cell. Biochem. 2009, 107:224-232.
100. Luo Z.J., Seedhom B.B. Light and low-frequency pulsatile hydrostatic pressure enhances extracellular matrix formation by bone marrow mesenchymal cells: An in-vitro study with special reference to cartilage repair. Proc. Inst. Mech. Eng. H 2007, 221:499-507.
101. Luu Y.K., Capilla E., Rosen C.J., Gilsanz V., Pessin J.E., Judex S., Rubin C.T. Mechanical stimulation of mesenchymal stem cell proliferation and differentiation promotes osteogenesis while preventing dietary-induced obesity. J. Bone Miner. Res. 2009, 24:50-61.
102. Maes F., Ransbeeck P., van Oosterwyck H., Verdonck P. Modeling fluid flow through irregular scaffolds for perfusion bioreactors. Biotechnol. Bioeng. 2009, 103:621-630.
103. Malone A.M.D., Anderson C.T., Tummala P., Kwon R.Y., Johnston T.R., Stearns T., Jacobs C.R. Primary cilia mediate mechanosensing in bone cells by a calcium-independent mechanism. Proc. Natl. Acad. Sci. USA 2007, 104:13325-13330.
104. Marvel S., Okrasinski S., Bernacki S.H., Loboa E., Dayton P.A. The development and validation of a LIPUS system with preliminary observations of ultrasonic effects on human adult stem cells. IEEE Trans. Ultrason. Ferroelectr. Freq. Control 2010, 57:1977-1984.
105. Matsiko A., Edwards J., Reilly G.C. Human mesenchymal stem cell responses to steady and oscillatory fluid flow in a porous scaffold. Regen. Med. 2009, 4:S159.
106. Mauck R.L., Byers B.A., Yuan X., Tuan R.S. Regulation of cartilaginous ECM gene transcription by chondrocytes and MSCs in 3D culture in response to dynamic loading. Biomech. Model. Mechanobiol. 2007, 6:113-125.
107. Mauney J.R., Sjostorm S., Blumberg J., Horan R., O'Leary J.P., Vunjak-Novakovic G., Volloch V., Kaplan D.L. Mechanical stimulation promotes osteogenic differentiation of human bone marrow stromal cells on 3-D partially demineralized bone scaffolds in vitro. Calcif. Tissue Int. 2004, 74:458-468.
108. McBride S.H., Falls T., Tate M.L.K. Modulation of stem cell shape and fate B: Mechanical modulation of cell shape and gene expression. Tissue Eng. Part A 2008, 14:1573-1580.
109. McCoy R.J., O'Brien F.J. Influence of shear stress in perfusion bioreactor cultures for the development of three-dimensional bone tissue constructs: A review. Tissue Eng. Part B Rev. 2010, 16:587-601.
110. McGarry J.G., Klein-Nulend J., Prendergast P.J. The effect of cytoskeletal disruption on pulsatile fluid flow-induced nitric oxide and prostaglandin E-2 release in osteocytes and osteoblasts. Biochem. Biophys. Res. Commun. 2005, 330:341-348.
111. McMahon L.A., Reid A.J., Campbell V.A., Prendergast P.J. Regulatory effects of mechanical strain on the chondrogenic differentiation of MSCs in a collagen-GAG scaffold: Experimental and computational analysis. Ann. Biomed. Eng. 2008, 36:185-194.
112. Meirelles L.D., Fontes A.M., Covas D.T., Caplan A.I. Mechanisms involved in the therapeutic properties of mesenchymal stem cells. Cytokine Growth Factor Rev. 2009, 20:419-427.
113. Miyanishi K., Trindade M.C.D., Lindsey D.P., Beaupre G.S., Carter D.R., Goodman S.B., Schurman D.J., Smith R.L. Dose- and time-dependent effects of cyclic hydrostatic pressure on transforming growth factor-beta 3-induced chondrogenesis by adult human mesenchymal stem cells in vitro. Tissue Eng. 2006, 12:2253-2262.
114. Miyanishi K., Trindade M.C.D., Lindsey D.P., Beaupre G.S., Carter D.R., Goodman S.B., Schurman D.J., Smith R.L. Effects of hydrostatic pressure and transforming growth factor-beta 3 on adult human mesenchymal stem cell chondrogenesis in vitro. Tissue Eng. 2006, 12:1419-1428.
115. Morgan E.F., Gleason R.E., Hayward L.N.M., Leong P.L., Palomares K.T.S. Mechanotransduction and fracture repair. J. Bone Joint. Surg. Am. 2008, 90A:25-30.
116. Morris H.L., Reed C.I., Haycock J.W., Reilly G.C. Mechanisms of fluid-flow-induced matrix production in bone tissue engineering. Proc. Inst. Mech. Eng. H 2010, 224:1509-1521.
117. Mouw J.K., Connelly J.T., Wilson C.G., Michael K.E., Levenston M.E. Dynamic compression regulates the expression and synthesis of chondrocyte-specific matrix molecules in bone marrow stromal cells. Stem Cells 2007, 25:655-663.
118. Murugan R., Ramakrishna S. Design strategies of tissue engineering scaffolds with controlled fiber orientation. Tissue Eng. 2007, 13:1845-1866.
119. Na K., Choi S.J., Kim S., Sun B.K., Woo D.G., Chung H.M., Park K.H. Enhancement of cell proliferation and differentiation by combination of ascorbate and dexamethasone in thermo-reversible hydrogel constructs embedded with rabbit chondrocytes. Biotechnol. Lett. 2007, 29:1453-1457.
120. Nerurkar N.L., Sen S., Baker B.M., Elliott D.M., Mauck R.L. Dynamic culture enhances stem cell infiltration and modulates extracellular matrix production on aligned electrospun nanofibrous scaffolds. Acta Biomater. 2011, 7:485-491.
121. Ngiam M., Liao S., Jie T.O.J., Sui X.D., Dong Y.X., Ramakrishna S., Chan C.K. Effects of mechanical stimulation in osteogenic differentiation of bone marrow-derived mesenchymal stem cells on aligned nanofibrous scaffolds. J. Bioact. Compat. Polym. 2011, 26:56-70.
122. Nirmalanandhan V.S., Juncosa-Melvin N., Shearn J.T., Boivin G.P., Galloway M.T., Gooch C., Bradica G., Butler D.L. Combined effects of scaffold stiffening and mechanical preconditioning cycles on construct biomechanics, gene Expression, and tendon repair biomechanics. Tissue Eng. Part A 2009, 15:2103-2111.
123. Nombela-Arrieta C., Ritz J., Silberstein L.E. The elusive nature and function of mesenchymal stem cells. Nat. Rev. Mol. Cell Biol. 2011, 12:126-131.
124. Nomura S., Takano-Yamamoto T. Molecular events caused by mechanical stress in bone. Matrix Biol. 2000, 19:91-96.
125. Ogawa R., Mizuno S., Murphy G.F., Orgill D.P. The effect of hydrostatic pressure on three-dimensional chondroinduction of human adipose-derived stem cells. Tissue Eng. Part A 2009, 15:2937-2945.
126. Orr A.W., Helmke B.P., Blackman B.R., Schwartz M.A. Mechanisms of mechanotransduction. Dev. Cell 2006, 10:11-20.
127. Osyczka A.M., Leboy P.S. Bone morphogenetic protein regulation of early osteoblast genes in human marrow stromal cells is mediated by extracellular signal-regulated kinase and phosphatidylinositol 3-kinase signaling. Endocrinology 2005, 146:3428-3437.
128. Ozcivici E., Luu Y.K., Rubin C.T., Judex S. Low-level vibrations retain bone marrow's osteogenic potential and augment recovery of trabecular bone during reambulation. PLoS One 2010, 5:e11178.
129. Pedersen J.A., Swartz M.A. Mechanobiology in the third dimension. Ann. Biomed. Eng. 2005, 33:1469-1490.
130. Pelham R.J., Wang Y.L. High resolution detection of mechanical forces exerted by locomoting fibroblasts on the substrate. Mol. Biol. Cell 1999, 10:935-945.
131. Plunkett N.A., Partap S., O'Brien F.J. Osteoblast response to rest periods during bioreactor culture of collagen-glycosaminoglycan scaffolds. Tissue Eng. Part A 2010, 16:943-951.
132. Pogue R., Lyons K. BMP signaling in the cartilage growth plate. Current Topics in Developmental Biology 2006, Vol. 76:1-48. Elsevier Inc., San Diego.
133. Porter R.M., Huckle W.R., Goldstein A.S. Effect of dexamethasone withdrawal on osteoblastic differentiation of bone marrow stromal cells. J. Cell. Biochem. 2003, 90:13-22.
134. Rehman J., Traktuev D., Li J.L., Merfeld-Clauss S., Temm-Grove C.J., Bovenkerk J.E., Pell C.L., Johnstone B.H., Considine R.V., March K.L. Secretion of angiogenic and antiapoptotic factors by human adipose stromal cells. Circulation 2004, 109:1292-1298.
135. Reilly G.C., Engler A.J. Intrinsic extracellular matrix properties regulate stem cell differentiation. J. Biomech. 2010, 43:55-62.
136. Reilly G., Haut T., Yellowley C., Donahue H., Jacobs C. Fluid flow induced PGE(2) release by bone cells is reduced by glycocalyx degradation whereas calcium signals are not. Biorheology 2003, 40:591-603.
137. Roshan-Ghias A., Terrier A., Bourban P.E., Pioletti D.P. In vivo cyclic loading as a potent stimulatory signal for bone formation inside tissue engineering scaffolds. Eur. Cells Mater. 2010, 19:41-49.
138. Rubin J., Rubin C., Jacobs C.R. Molecular pathways mediating mechanical signaling in bone. Gene 2006, 367:1-16.
139. Rubin C.T., Capilla E., Luu Y.K., Busa B., Crawford H., Nolan D.J., Mittal V., Rosen C.J., Pessin J.E., Judex S. Adipogenesis is inhibited by brief, daily exposure to high-frequency, extremely low-magnitude mechanical signals. Proc. Natl. Acad. Sci. USA 2007, 104:17879-17884.
140. Rui Y.F., Lui P.P.Y., Ni M., Chan L.S., Lee Y.W., Chan K.M. Mechanical loading increased BMP-2 expression which promoted osteogenic differentiation of tendon-derived stem cells. J. Orthop. Res. 2011, 29:390-396.
141. 2 in the recruitment of bone marrow mesenchymal cells to the osteoblastic lineage: Positive and negative effects. Calcif. Tissue Int. 1996, 59:154-162.
142. Sen B., Xie Z.H., Case N., Ma M.Y., Rubin C., Rubin J. Mechanical strain inhibits adipogenesis in mesenchymal stem cells by stimulating a durable beta-catenin signal. Endocrinology 2008, 149:6065-6075.
143. Sen B., Xie Z.H., Case N., Styner M., Rubin C.T., Rubin J. Mechanical signal influence on mesenchymal stem cell fate is enhanced by incorporation of refractory periods into the loading regimen. J. Biomech. 2011, 44:593-599.
144. Seong J.M., Kim B.C., Park J.H., Kwon I.K., Mantalaris A., Hwang Y.S. Stem cells in bone tissue engineering. Biomed. Mater. 2010, 5:062001.
145. Sharp L.A., Lee Y.W., Goldstein A.S. Effect of low-frequency pulsatile flow on expression of osteoblastic genes by bone marrow stromal cells. Ann. Biomed. Eng. 2009, 37:445-453.
146. Shim W.S.N., Jiang S., Wong P., Tan J., Chua Y.L., Tan Y.S., Sin Y.K., Lim C.H., Chua T., Teh M., Liu T.C., Simr E. Ex vivo differentiation of human adult bone marrow stem cells into cardiomyocyte-like cells. Biochem. Biophys. Res. Commun. 2004, 324:481-488.
147. Sikavitsas V.I., Bancroft G.N., Holtorf H.L., Jansen J.A., Mikos A.G. Mineralized matrix deposition by marrow stromal osteoblasts in 3D perfusion culture increases with increasing fluid shear forces. Proc. Natl. Acad. Sci. USA 2003, 100:14683-14688.
148. Sikavitsas V.I., Bancroft G.N., Lemoine J.J., Liebschner M.A.K., Dauner M., Mikos A.G. Flow perfusion enhances the calcified matrix deposition of marrow stromal cells in biodegradable nonwoven fiber mesh scaffolds. Ann. Biomed. Eng. 2005, 33:63-70.
149. Simmons C.A., Matlis S., Thornton A.J., Chen S.Q., Wang C.Y., Mooney D.J. Cyclic strain enhances matrix mineralization by adult human mesenchymal stem cells via the extracellular signal-regulated kinase (ERK1/2) signaling pathway. J. Biomech. 2003, 36:1087-1096.
150. Sioud M., Mobergslien A., Boudabous A., Floisand Y. Mesenchymal stem cell-mediated T cell suppression occurs through secreted galectins. Int. J. Oncol. 2011, 38:385-390.
151. Sittichockechaiwut A., Scutt A., Ryan A., Bonewald L., Reilly G. Use of rapidly mineralising osteoblasts and short periods of mechanical loading to accelerate matrix maturation in 3D scaffolds. Bone 2009, 44:822-829.
152. Sittichokechaiwut A., Edwards J., Scutt A., Reilly G. Short bouts of mechanical loading are as effective as dexamethasone at inducing matrix production by human bone marrow mesenchymal stem cells. Eur. Cells Mater. 2010, 20:45-57.
153. Soncini M., Vertua E., Gibelli L., Zorzi F., Denegri M., Albertini A., Wengler G.S., Parolini O. Isolation and characterization of mesenchymal cells from human fetal membranes. J. Tissue Eng. Regen. Med. 2007, 1:296-305.
154. Srinivasan S., Weimer D.A., Agans S.C., Bain S.D., Gross T.S. Low-magnitude mechanical loading becomes osteogenic when rest is inserted between each load cycle. J. Bone Miner. Res. 2002, 17:1613-1620.
155. Stewart A.A., Byron C.R., Pondenis H.C., Stewart M.C. Effect of dexamethasone supplementation on chondrogenesis of equine mesenchymal stem cells. Am. J. Vet. Res. 2008, 69:1013-1021.
156. Stock U.A., Vacanti J.P. Tissue engineering: Current state and prospects. Annu. Rev. Med. 2001, 52:443-451.
157. Sumanasinghe R.D., Bernacki S.H., Loboa E.G. Osteogenic differentiation of human mesenchymal stem cells in collagen matrices: Effect of uniaxial cyclic tensile strain on bone morphogenetic protein (BMP-2) mRNA expression. Tissue Eng. 2006, 12:3459-3465.
158. Takada I., Kouzmenko A.P., Kato S. PPAR-gamma signaling crosstalk in mesenchymal stem cells. PPAR Res. 2010, Article No.: 341671.
159. Tanaka S.M., Sun H.B., Roeder R.K., Burr D.B., Turner C.H., Yokota H. Osteoblast responses one hour after load-induced fluid flow in a three-dimensional porous matrix. Calcif. Tissue Int. 2005, 76:261-271.
160. Terraciano V., Hwang N., Moroni L., Park H.B., Zhang Z., Mizrahi J., Seliktar D., Elisseeff J. Differential response of adult and embryonic mesenchymal progenitor cells to mechanical compression in hydrogels. Stem Cells 2007, 25:2730-2738.
161. Thompson M.S., Epari D.R., Bieler F., Duda G.N. In vitro models for bone mechanobiology: Applications in bone regeneration and tissue engineering. Proc. Inst. Mech. Eng. H 2010, 224:1533-1541.
162. Thorpe S.D., Buckley C.T., Vinardell T., O'Brien F.J., Campbell V.A., Kelly D.J. The response of bone marrow-derived mesenchymal stem cells to dynamic compression following TGF-beta 3 induced chondrogenic differentiation. Ann. Biomed. Eng. 2010, 38:2896-2909.
163. Titushkin I., Sun S., Shin J., Cho M. Physicochemical control of adult stem cell differentiation: Shedding light on potential molecular mechanisms. J. Biomed. Biotechnol. 2010, 2010. Article No.: 743476.
164. Tuli R., Tuli S., Nandi S., Huang X.X., Manner P.A., Hozack W.J., Danielson K.G., Hall D.J., Tuan R.S. Transforming growth factor-beta-mediated chondrogenesis of human mesenchymal progenitor cells involves N-cadherin and mitogenactivated protein kinase and Wnt signaling cross-talk. J. Biol. Chem. 2003, 278:41227-41236.
165. Tummala P., Arnsdorf E.J., Jacobs C.R. The role of primary cilia in mesenchymal stem cell differentiation: A pivotal switch in guiding lineage commitment. Cell. Mol. Bioeng. 2010, 3:207-212.
166. van Beuningen H.M., Glansbeek H.L., van der Kraan P.M., van den Berg W.B. Differential effects of local application of BMP-2 or TGF-beta 1 on both articular cartilage composition and osteophyte formation. Osteoarthritis Cartilage 1998, 6:306-317.
167. van Eijk F., Saris D.B.F., Creemers L.B., Riesle J., Willems W.J., van Blitterswijk C.A., Verbout A.J., Dhert W.J.A. The effect of timing of mechanical stimulation on proliferation and differentiation of goat bone marrow stem cells cultured on braided PLGA scaffolds. Tissue Eng. Part A 2008, 14:1425-1433.
168. VanGordon S.B., Voronov R.S., Blue T.B., Shambaugh R.L., Papavassiliou D.V., Sikavitsas V.I. Effects of scaffold architecture on preosteoblastic cultures under continuous fluid shear. Ind. Eng. Chem. Res. 2011, 50:620-629.
169. Vater C., Kasten P., Stiehler M. Culture media for the differentiation of mesenchymal stromal cells. Acta Biomater. 2011, 7:463-477.
170. Vogel V. Mechanotransduction involving multimodular proteins: Converting force into biochemical signals. Annu. Rev. Biophys. Biomol. Struct. 2006, 35:459-488.
171. Wagner D.R., Lindsey D.P., Li K.W., Tummala P., Chandran S.E., Smith R.L., Longaker M.T., Carter D.R., Beaupre G.S. Hydrostatic pressure enhances chondrogenic differentiation of human bone marrow stromal cells in osteochondrogenic medium. Ann. Biomed. Eng. 2008, 36:813-820.
172. Wang N., Butler J.P., Ingber D.E. Mechanotransduction across the cell surface and through the cytoskeleton. Science 1993, 260:1124-1127.
173. Watanabe Y., Matsushita T., Bhandari M., Zdero R., Schemitsch E.H. Ultrasound for fracture healing: Current evidence. J. Orthop. Trauma 2010, 24:S56-S61.
174. Weinbaum S., Cowin S.C., Zeng Y. A model for the excitation of osteocytes by mechanical loading-induced bone fluid shear stresses. J. Biomech. 1994, 27:339-360.
175. Weinbaum S., Tarbell J.M., Damiano E.R. The structure and function of the endothelial glycocalyx layer. Annu. Rev. Biomed. Eng. 2007, 9:121-167.
176. Willie B.M., Petersen A., Schmidt-Bleek K., Cipitria A., Mehta M., Strube P., Lienau J., Wildemann B., Fratzl P., Duda G. Designing biomimetic scaffolds for bone regeneration: Why aim for a copy of mature tissue properties if nature uses a different approach?. Soft Matter 2010, 6:4976-4987.
177. Xie L.Q., Jacobson J.M., Choi E.S., Busa B., Donahue L.R., Miller L.M., Rubin C.T., Judex S. Low-level mechanical vibrations can influence bone resorption and bone formation in the growing skeleton. Bone 2006, 39:1059-1066.
178. Yang D.C., Tsay H.J., Lin S.Y., Chiou S.H., Li M.J., Chang T.J., Hung S.C. cAMP/PKA regulates osteogenesis, adipogenesis and ratio of RANKL/OPG mRNA expression in mesenchymal stem cells by suppressing leptin. PLoS One 2008, 3:e1540.
179. Yang X.M., Gong P., Lin Y.F., Zhang L.R., Li X.Y., Yuan Q.A., Tan Z., Wang Y.Y., Man Y., Tang H. Cyclic tensile stretch modulates osteogenic differentiation of adipose-derived stem cells via the BMP-2 pathway. Arch. Med. Sci. 2010, 6:152-159.
180. Yin Z., Chen X., Chen J.L., Ouyang H.W. Stem cells for tendon tissue engineering and regeneration. Expert Opin. Biol. Ther. 2010, 10:689-700.
181. You J., Reilly G., Zhen X., Yeollowley C., Chen Q., Donahue H., Jacobs C. Osteopontin gene regulation by oscillatory fluid flow via intracellular calcium mobilization and activation of mitogen-activated protein kinase in MC3T3-E1 osteoblasts. J. Biol. Chem. 2001, 276:13365-13371.
182. You L., Temiyasathit S., Coyer S.R., Garcia A.J., Jacobs C.R. Bone cells grown on micropatterned surfaces are more sensitive to fluid shear stress. Cell. Mol. Bioeng. 2008, 1:182-188.
183. Yourek G., Hussain M.A., Mao J.J. Cytoskeletal changes of mesenchymal stem cells during differentiation. Asaio J. 2007, 53:219-228.
184. Yourek G., McCormick S., Mao J., Reilly G. Shear stress induces osteogenic differentiation of human mesenchymal stem cells. Regen. Med. 2010, 5:713-724.
185. Zeiter S., Lezuo P., Ito K. Effect of TGF beta(1), BMP-2 and hydraulic pressure on chondrogenic differentiation of bovine bone marrow mesenchymal stromal cells. Biorheology 2009, 46:45-55.
186. Zhang L., Tran N., Chen H.Q., Kahn C.J.F., Marchal S., Groubatch F., Wang X. Time-related changes in expression of collagen types I and III and of tenascin-C in rat bone mesenchymal stem cells under co-culture with ligament fibroblasts or uniaxial stretching. Cell Tissue Res. 2008, 332:101-109.
187. Zhao F., Chella R., Ma T. Effects of shear stress on 3-D human mesenchymal stem cell construct development in a perfusion bioreactor system: Experiments and hydrodynamic modeling. Biotechnol. Bioeng. 2007, 96:584-595.
188. Zhou X.Z., Liu D.W., You L.D., Wang L.Y. Quantifying fluid shear stress in a rocking culture dish. J. Biomech. 2010, 43:1598-1602.
189. Zuk P.A., Zhu M., Mizuno H., Huang J., Futrell J.W., Katz A.J., Benhaim P., Lorenz H.P., Hedrick M.H. Multilineage cells from human adipose tissue: Implications for cell-based therapies. Tissue Eng. 2001, 7:211-228.
190. Zvaifler N.J., Marinova-Mutafchieva L., Adams G., Edwards C.J., Moss J., Burger J.A., Maini R.N. Mesenchymal precursor cells in the blood of normal individuals. Arthritis Res. 2000, 2:477-488.